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LINE-1 retrotransposons facilitate horizontal gene transfer into poxviruses.

ABSTRACT: There is ample phylogenetic evidence that many critical virus functions, like immune evasion, evolved by the acquisition of genes from their hosts through horizontal gene transfer (HGT). However, the lack of an experimental system has prevented a mechanistic understanding of this process. We developed a model to elucidate the mechanisms of HGT into vaccinia virus, the prototypic poxvirus. All identified gene capture events showed signatures of long interspersed nuclear element-1 (LINE-1)-mediated retrotransposition, including spliced-out introns, polyadenylated tails, and target site duplications. In one case, the acquired gene integrated together with a polyadenylated host U2 small nuclear RNA. Integrations occurred across the genome, in some cases knocking out essential viral genes. These essential gene knockouts were rescued through a process of complementation by the parent virus followed by nonhomologous recombination during serial passaging to generate a single, replication-competent virus. This work links multiple evolutionary mechanisms into one adaptive cascade and identifies host retrotransposons as major drivers for virus evolution.

SUBMITTER: Rahman MJ

PROVIDER: S-EPMC9578709 | biostudies-literature | 2022 Sep

REPOSITORIES: biostudies-literature

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LINE-1 retrotransposons facilitate horizontal gene transfer into poxviruses.

Rahman M Julhasur MJ Haller Sherry L SL Stoian Ana M M AMM Li Jie J Brennan Greg G Rothenburg Stefan S

eLife 20220907

There is ample phylogenetic evidence that many critical virus functions, like immune evasion, evolved by the acquisition of genes from their hosts through horizontal gene transfer (HGT). However, the lack of an experimental system has prevented a mechanistic understanding of this process. We developed a model to elucidate the mechanisms of HGT into vaccinia virus, the prototypic poxvirus. All identified gene capture events showed signatures of long interspersed nuclear element-1 (LINE-1)-mediate ...[more]

PMID: 36069678

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Project description:BackgroundHorizontal transfer (HT) of genetic materials is increasingly being found in both animals and plants and mainly concerns transposable elements (TEs). Many crustaceans have big genome sizes and are thus likely to harbor high TE contents. Their habitat might offer them ample opportunities to exchange genetic materials with organisms that are ecologically close but taxonomically distant to them.ResultsIn this study, we analyzed the transcriptome of Pacific white shrimp (Litopenaeus vannamei), an important economic crustacean, to explore traces of HT events. From a collection of newly assembled transcripts, we identified 395 high reliable TE transcripts, most of which were retrotransposon transcripts. One hundred fifty-seven of those transcripts showed highest similarity to sequences from non-arthropod organisms, including ray-finned fishes, mollusks and putative parasites. In total, 16 already known L. vannamei TE families are likely to be involved in horizontal transfer events. Phylogenetic analyses of 10?L. vannamei TE families and their homologues (protein sequences) revealed that L. vannamei TE families were generally more close to sequences from aquatic species. Furthermore, TEs from other aquatic species also tend to group together, although they are often distantly related in taxonomy. Sequences from parasites and microorganisms were also widely present, indicating their possible important roles in HT events. Expression profile analyses of transcripts in two NCBI BioProjects revealed that transcripts involved in HT events are likely to play important roles in antiviral immunity. More specifically, those transcripts might act as inhibitors of antiviral immunity.ConclusionsClose ecological relationship, especially predation, might greatly facilitate HT events among aquatic species. This could be achieved through exchange of parasites and microorganisms, or through direct DNA flow. The occurrence of HT events may be largely incidental, but the effects could be beneficial for recipients.

Dataset Information

LINE-1 retrotransposons facilitate horizontal gene transfer into poxviruses.

Publications

LINE-1 retrotransposons facilitate horizontal gene transfer into poxviruses.

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